The molecular pathogenesis of myelodysplastic syndromes

Cancer Biology and Therapy

Volumn 10, Issue 4, 2010, Pages 309-319

  Davids, Matthew S ^a   Steensma, David P ^a  

^a HARVARD MEDICAL SCHOOL   (United States)

Author keywords

Cytogenetic; Genetic; Hematopoiesis; Myelodysplastic syndrome; Pathogenesis

Indexed keywords

ASXL1 PROTEIN; ATRX PROTEIN; CBL PROTEIN; CD135 ANTIGEN; CDC25C PROTEIN; CELL PROTEIN; DNA; IMMEDIATE EARLY RESPONSE 3 PROTEIN; OSTEONECTIN; PHOSPHOPROTEIN PHOSPHATASE 2; PROTEIN P53; PROTEIN TYROSINE PHOSPHATASE; RAS PROTEIN; RIBOSOMAL PROTEIN S14; RIBOSOME PROTEIN; TET2 PROTEIN; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR RUNX1; TUMOR SUPPRESSOR PROTEIN; UNCLASSIFIED DRUG;

APOPTOSIS; CYTOGENETICS; CYTOLOGY; DISEASE COURSE; DNA REPAIR; GENE EXPRESSION; GENE MUTATION; GENE REARRANGEMENT; GENETIC ASSOCIATION; HETEROZYGOSITY; HUMAN; MYELODYSPLASTIC SYNDROME; OXIDATIVE STRESS; PATHOGENESIS; PHENOTYPE; POINT MUTATION; REVIEW;

APOPTOSIS; BONE MARROW DISEASES; CHROMOSOME ABERRATIONS; DNA REPAIR; HAPLOINSUFFICIENCY; HEMOGLOBINURIA, PAROXYSMAL; HUMANS; LEUKEMIA, MYELOID, ACUTE; MYELODYSPLASTIC-MYELOPROLIFERATIVE DISEASES; OXIDATIVE STRESS; POINT MUTATION; PROTEIN BIOSYNTHESIS; TRANSLOCATION, GENETIC;

EID: 77957146789     PISSN: 15384047     EISSN: 15558576     Source Type: Journal    
DOI: 10.4161/cbt.10.4.12612     Document Type: Review

References (102)

1. Nimer SD. Myelodysplastic syndromes. Blood 2008; 111:4841-51.
2. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, et al. eds. WHO Classification of Tumours of Haematopoietic and Lymphoid Tissues, Fourth Edition. Lyon: IARC Press 2008.
3. List A, Dewald G, Bennett J, Giagounidis A, Raza A, Feldman E, et al. Lenalidomide in the myelodysplastic syndrome with chromosome 5q deletion. N Engl J Med 2006; 355:1456-65. (Pubitemid 44511560)
4. Ley TJ, Mardis ER, Ding L, Fulton B, McLellan MD, Chen K, et al. DNA sequencing of a cytogenetically normal acute myeloid leukaemia genome. Nature 2008; 456:66-72.
5. Mardis ER, Ding L, Dooling DJ, Larson DE, McLellan MD, Chen K, et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med 2009; 361:1058-66.
6. Levine RL, Wadleigh M, Cools J, Ebert BL, Wernig G, Huntly BJP, et al. Activating mutation in the tyrosine kinase JAK2 in polycythemia vera, essential thrombocythemia and agnogenic myeloid metaplasia. Cancer Cell 2005; 7:387-97.
7. Kumano K, Kurokawa M. The role of Runx1/AML1 and Evi-1 in the regulation of hematopoietic stem cells. J Cell Physiol 2010; 222:282-5.
8. Growney JD, Shigematsu H, Li Z, Lee BH, Adelsperger J, Rowan R, et al. Loss of Runx1 perturbs adult hematopoiesis and is associated with a myeloproliferative phenotype. Blood 2005; 106:494-504. (Pubitemid 40981243)
9. Harada Y, Harada H. Molecular pathways mediating MDS/AML with focus on AML1/RUNX1 point mutations. J Cell Physiol 2009; 220:16-20.
10. Steensma DP, Gibbons RJ, Mesa RA, Tefferi A, Higgs DR. Somatic point mutations in RUNX1/CBFA2/AML1 are common in high-risk myelodysplastic syndrome, but not in myelofibrosis with myeloid metaplasia. Eur J Haematol 2005; 74:47-53.
11. Harada H, Harada Y, Niimi H, Kyo T, Kimura A, Inaba T. High incidence of somatic mutations in the AML1/RUNX1 gene in myelodysplastic syndrome and low blast percentage myeloid leukemia with myelodysplasia. Blood 2004; 103:2316-24. (Pubitemid 38326252)
12. Watanabe-Okochi N, Kitaura J, Ono R, Harada H, Harada Y, Komeno Y, et al. AML1 mutations induced MDS and MDS/AML in a mouse BMT model. Blood 2008; 111:4297-308.
13. Matheny CJ, Speck ME, Cushing PR, Zhou Y, Corpora T, Regan M, et al. Disease mutations in RUNX1 and RUNX2 create nonfunctional, dominant-negative or hypomorphic alleles. EMBO J 2007; 26:1163-75.
14. Owen CJ, Toze CL, Koochin A, Forrest DL, Smith CA, Stevens JM, et al. Five new pedigrees with inherited RUNX1 mutations causing familial platelet disorder with propensity to myeloid malignancy. Blood 2008; 112:4639-45.
15. Soderholm J, Kobayashi H, Mathieu C, Rowley JD, Nucifora G. The leukemia-associated gene MDS1/EVI1 is a new type of GATA-binding transactivator. Leukemia 1997; 11:352-8. (Pubitemid 27120983)
16. Yamamoto K, Nagata K, Tsurukubo Y, Morishita K, Hamaguchi H. A novel translocation t(3;22)(q21;q11) involving 3q21 in myelodysplastic syndrome-derived overt leukemia with thrombocytosis. Leuk Res 2000; 24:453-7.
17. Du Y, Wang K, Fang H, Li J, Xiao D, Zheng P, et al. Coordination of intrinsic, extrinsic and endoplasmic reticulum-mediated apoptosis by imatinib mesylate combined with arsenic trioxide in chronic myeloid leukemia. Blood 2006; 107:1582-90.
18. Vardiman JW, Thiele J, Arber DA, Brunning RD, Borowitz MJ, Porwit A, et al. The 2008 revision of the World Health Organization (WHO) classification of myeloid neoplasms and acute leukemia: rationale and important changes. Blood 2009; 114:937-51.
19. Tahiliani M, Koh KP, Shen Y, Pastor WA, Bandukwala H, Brudno Y, et al. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 2009; 324:930-5.
20. Langemeijer SM, Kuiper RP, Berends M, Knops R, Aslanyan MG, Massop M, et al. Acquired mutations in TET2 are common in myelodysplastic syndromes. Nat Genet 2009; 41:838-42.
21. Kosmider O, Gelsi-Boyer V, Cheok M, Grabar S, Della-Valle V, Picard F, et al. TET2 mutation is an independent favorable prognostic factor in myelodysplastic syndromes (MDSs). Blood 2009; 114:3285-91.
22. Jankowska AM, Szpurka H, Tiu RV, Makishima H, Afable M, Huh J, et al. Loss of heterozygosity 4q24 and TET2 mutations associated with myelodysplastic/myeloproliferative neoplasms. Blood 2009; 113:6403-10.
23. Delhommeau F, Dupont S, Della Valle V, James C, Trannoy S, Masse A, et al. Mutation in TET2 in myeloid cancers. N Engl J Med 2009; 360:2289-301.
24. Fenaux P, Mufti GJ, Hellstrom-Lindberg E, Santini V, Finelli C, Giagounidis A, et al. Efficacy of azacitidine compared with that of conventional care regimens in the treatment of higher-risk myelodysplastic syndromes: a randomised, open-label, phase III study. Lancet Oncol 2009; 10:223-32.
25. Cho YS, Kim EJ, Park UH, Sin HS, Um SJ. Additional sex comb-like 1 (ASXL1), in cooperation with SRC-1, acts as a ligand-dependent coactivator for retinoic acid receptor. J Biol Chem 2006; 281:17588-98.
26. Lee SW, Cho YS, Na JM, Park UH, Kang M, Kim EJ, et al. ASXL1 represses retinoic acid receptor-mediated transcription through associating with HP1 and LSD1. J Biol Chem 2009; 285:18-29.
27. Murati A, Gelsi-Boyer V, Adelaide J, Perot C, Talmant P, Giraudier S, et al. PCM1-JAK2 fusion in myeloproliferative disorders and acute erythroid leukemia with t(8;9) translocation. Leukemia 2005; 19:1692-6.
28. Boultwood J, Perry J, Pellagatti A, Fernandez-Mercado M, Fernandez-Santamaria C, Calasanz MJ, et al. Frequent mutation of the polycomb-associated gene ASXL1 in the myelodysplastic syndromes and in acute myeloid leukemia. Leukemia 2010; 24:1062-5.
29. Fisher CL, Pineault N, Brookes C, Helgason CD, Ohta H, Bodner C, et al. Loss-of-function Additional sex combs like 1 mutations disrupt hematopoiesis but do not cause severe myelodysplasia or leukemia. Blood 2010; 115:38-46.
30. Draptchinskaia N, Gustavsson P, Andersson B, Pettersson M, Willig TN, Dianzani I, et al. The gene encoding ribosomal protein S19 is mutated in Diamond-Blackfan anaemia. Nat Genet 1999; 21:169-75.
31. Valencia A, Cervera J, Such E, Sanz MA, Sanz GF. Lack of RPS14 promoter aberrant methylation supports the haploinsufficiency model for the 5q- syndrome. Blood 2008; 112:918.
32. + cells is associated with survival of patients suffering from myelodysplastic syndrome. Int J Hematol 2009; 89:173-87.
33. Narla A, Ebert BL. Ribosomopathies: human disorders of ribosome dysfunction. Blood 2010; 115:3196-205.
34. Pellagatti A, Marafioti T, Paterson JC, Barlow JL, Drynan LF, Giagounidis A, et al. Induction of p53 and upregulation of the p53 pathway in the human 5q- syndrome. Blood 2010; 115:2721-3.
35. Barlow JL, Drynan LF, Hewett DR, Holmes LR, Lorenzo-Abalde S, Lane AL, et al. A p53-dependent mechanism underlies macrocytic anemia in a mouse model of human 5q- syndrome. Nat Med 2010; 16:59-66.
36. Joslin JM, Fernald AA, Tennant TR, Davis EM, Kogan SC, Anastasi J, et al. Haploinsufficiency of EGR1, a candidate gene in the del(5q), leads to the development of myeloid disorders. Blood 2007; 110:719-26. (Pubitemid 47105411)
37. Starczynowski DT, Kuchenbauer F, Argiropoulos B, Sung S, Morin R, Muranyi A, et al. Identification of miR-145 and miR-146a as mediators of the 5q- syndrome phenotype. Nat Med 2010; 16:49-58.
38. Wei S, Chen X, Rocha K, Epling-Burnette PK, Djeu JY, Liu Q, et al. A critical role for phosphatase haplodeficiency in the selective suppression of deletion 5q MDS by lenalidomide. Proc Natl Acad Sci U S A2009; 106:12974-9.
39. List A, Rocha K, Zhang L, Komrokji R, Clark J, Caceres G, et al. Secondary Resistance to Lenalidomide in Del(5q) MDS is Associated with CDC25C and PP2A Overexpression. Blood (ASH Annual Meeting Extracts) 2009.
40. Caudill JS, Porcher JC, Steensma DP. Aberrant pre-mRNA splicing of a highly conserved cell cycle regulator, CDC25C, in myelodysplastic syndromes. Leuk Lymphoma 2008; 49:989-93.
41. + cells in patients with the 5q- syndrome. Br J Haematol 2007; 139:578-89.
42. Raaijmakers MH, Mukherjee S, Guo S, Zhang S, Kobayashi T, Schoonmaker JA, et al. Bone progenitor dysfunction induces myelodysplasia and secondary leukaemia. Nature 464:852-7.
43. Thien CB, Langdon WY. Cbl: many adaptations to regulate protein tyrosine kinases. Nat Rev Mol Cell Biol 2001; 2:294-307.
44. Sanada M, Suzuki T, Shih LY, Otsu M, Kato M, Yamazaki S, et al. Gain-of-function of mutated C-CBL tumour suppressor in myeloid neoplasms. Nature 2009; 460:904-8.
45. Dunbar AJ, Gondek LP, O'Keefe CL, Makishima H, Rataul MS, Szpurka H, et al. 250K single nucleotide polymorphism array karyotyping identifies acquired uniparental disomy and homozygous mutations, including novel missense substitutions of c-Cbl, in myeloid malignancies. Cancer Res 2008; 68:10349-57.
46. Makishima H, Cazzolli H, Szpurka H, Dunbar A, Tiu R, Huh J, et al. Mutations of e3 ubiquitin ligase cbl family members constitute a novel common pathogenic lesion in myeloid malignancies. J Clin Oncol 2009; 27:6109-16.
47. Christiansen DH, Andersen MK, Pedersen-Bjergaard J. Mutations with loss of heterozygosity of p53 are common in therapy-related myelodysplasia and acute myeloid leukemia after exposure to alkylating agents and significantly associated with deletion or loss of 5q, a complex karyotype and a poor prognosis. J Clin Oncol 2001; 19:1405-13.
48. Kita-Sasai Y, Horiike S, Misawa S, Kaneko H, Kobayashi M, Nakao M, et al. International prognostic scoring system and TP53 mutations are independent prognostic indicators for patients with myelodysplastic syndrome. Br J Haematol 2001; 115:309-12.
49. Link PA, Baer MR, James SR, Jones DA, Karpf AR. p53-inducible ribonucleotide reductase (p53R2/RRM2B) is a DNA hypomethylation-independent decitabine gene target that correlates with clinical response in myelodysplastic syndrome/acute myelogenous leukemia. Cancer Res 2008; 68:9358-66.
50. Jadersten M, Saft L, Pellagatti A, Gohring G, Wainscoat JS, Boultwood J, et al. Clonal heterogeneity in the 5q-syndrome: p53 expressing progenitors prevail during lenalidomide treatment and expand at disease progression. Haematologica 2009; 94:1762-6.
51. Steensma DP, Neiger JD, Porcher JC, Keats JJ, Bergsagel PL, Dennis TR, et al. Rearrangements and amplification of IER3 (IEX-1) represent a novel and recurrent molecular abnormality in myelodysplastic syndromes. Cancer Res 2009; 69:7518-23.
52. + cells from normal and myelodysplastic bone marrow. Blood 2002; 100:3553-60.
53. Gibbons RJ, Bachoo S, Picketts DJ, Aftimos S, Asenbauer B, Bergoffen J, et al. Mutations in transcriptional regulator ATRX establish the functional significance of a PHD-like domain. Nat Genet 1997; 17:146-8.
54. Gibbons RJ, Picketts DJ, Villard L, Higgs DR. Mutations in a putative global transcriptional regulator cause X-linked mental retardation with alpha-thalassemia (ATR-X syndrome). Cell 1995; 80:837-45.
55. Steensma DP, Porcher JC, Hanson CA, Lathrop CL, Hoyer JD, Lasho TA, et al. Prevalence of erythrocyte haemoglobin H inclusions in unselected patients with clonal myeloid disorders. Br J Haematol 2007; 139:439-42.
56. Steensma DP, Higgs DR, Fisher CA, Gibbons RJ. Acquired somatic ATRX mutations in myelodysplastic syndrome associated with alpha thalassemia (ATMDS) convey a more severe hematologic phenotype than germline ATRX mutations. Blood 2004; 103:2019-26.
57. Costa DB, Fisher CA, Miller KB, Pihan GA, Steensma DP, Gibbons RJ, et al. A novel mutation in the last exon of ATRX in a patient with alpha-thalassemia myelodysplastic syndrome. Eur J Haematol 2006; 76:432-5.
58. Steensma DP, Porcher JC, Litzow MR, Hogan WJ, Arora S, Van Laar ES. Assessment of ATRX expression in patients with myelodysplastic syndromes treated with decitabine. Leuk Res 2009; 33:81-2.
59. van Haaften G, Dalgliesh GL, Davies H, Chen L, Bignell G, Greenman C, et al. Somatic mutations of the histone H3K27 demethylase gene UTX in human cancer. Nat Genet 2009; 41:521-3.
60. Agger K, Cloos PA, Christensen J, Pasini D, Rose S, Rappsilber J, et al. UTX and JMJD3 are histone H3K27 demethylases involved in HOX gene regulation and development. Nature 2007; 449:731-4.
61. Constantinidou M, Chalevelakis G, Economopoulos T, Koffa M, Liloglou T, Anastassiou C, et al. Codon 12 ras mutations in patients with myelodysplastic syndrome: incidence and prognostic value. Ann Hematol 1997; 74:11-4.
62. Paquette RL, Landaw EM, Pierre RV, Kahan J, Lubbert M, Lazcano O, et al. N-ras mutations are associated with poor prognosis and increased risk of leukemia in myelodysplastic syndrome. Blood 1993; 82:590-9.
63. Kurzrock R, Albitar M, Cortes JE, Estey EH, Faderl SH, Garcia-Manero G, et al. Phase II study of R115777, a farnesyl transferase inhibitor, in myelodysplastic syndrome. J Clin Oncol 2004; 22:1287-92.
64. Abu-Duhier FM, Goodeve AC, Wilson GA, Gari MA, Peake IR, Rees DC, et al. FLT3 internal tandem duplication mutations in adult acute myeloid leukaemia define a high-risk group. Br J Haematol 2000; 111:190-5.
65. Horiike S, Yokota S, Nakao M, Iwai T, Sasai Y, Kaneko H, et al. Tandem duplications of the FLT3 receptor gene are associated with leukemic transformation of myelodysplasia. Leukemia 1997; 11:1442-6.
66. Georgiou G, Karali V, Zouvelou C, Kyriakou E, Dimou M, Chrisochoou S, et al. Serial determination of FLT3 mutations in myelodysplastic syndrome patients at diagnosis, follow up or acute myeloid leukaemia transformation: incidence and their prognostic significance. Br J Haematol 2006; 134:302-6.
67. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, Baldwin J, et al. Initial sequencing and analysis of the human genome. Nature 2001; 409:860-921.
68. Pappa V, Papageorgiou S, Kontsioti F, Papageorgiou E, Tsiotra P, Dervenoulas J, et al. Analysis of FLT3 gene mutations in de novo myelodysplastic syndromes. FLT3 internal tandem duplication detected in a case of refractory anemia. Leuk Lymphoma 2007; 48:2437-40.
69. Cavadini P, Biasiotto G, Poli M, Levi S, Verardi R, Zanella I, et al. RNA silencing of the mitochondrial ABCB7 transporter in HeLa cells causes an iron-deficient phenotype with mitochondrial iron overload. Blood 2007; 109:3552-9.
70. Boultwood J, Pellagatti A, Nikpour M, Pushkaran B, Fidler C, Cattan H, et al. The role of the iron transporter ABCB7 in refractory anemia with ring sideroblasts. PLoS ONE 2008; 3:1970.
71. Oscarson M, Zanger UM, Rifki OF, Klein K, Eichelbaum M, Meyer UA. Transcriptional profiling of genes induced in the livers of patients treated with carbamazepine. Clin Pharmacol Ther 2006; 80:440-56.
72. Nearman ZP, Szpurka H, Serio B, Warshawksy I, Theil K, Lichtin A, et al. Hemochromatosis-associated gene mutations in patients with myelodysplastic syndromes with refractory anemia with ringed sideroblasts. Am J Hematol 2007; 82:1076-9.
73. Tehranchi R, Invernizzi R, Grandien A, Zhivotovsky B, Fadeel B, Forsblom AM, et al. Aberrant mitochondrial iron distribution and maturation arrest characterize early erythroid precursors in low-risk myelodysplastic syndromes. Blood 2005; 106:247-53. (Pubitemid 40967200)
74. Nikpour M, Pellagatti A, Liu A, Karimi M, Malcovati L, Gogvadze V, et al. Gene expression profiling of erythroblasts from refractory anaemia with ring sideroblasts (RARS) and effects of G-CSF. Br J Haematol 2010; [Epub ahead of print].
75. Flores-Figueroa E, Gutierrez-Espindola G, Montesinos JJ, Arana-Trejo RM, Mayani H. In vitro characterization of hematopoietic microenvironment cells from patients with myelodysplastic syndrome. Leuk Res 2002; 26:677-86.
76. Kabutomori O, Kanakura Y, Iwatani Y. Marked decreases of total and immature reticulocytes in myelodysplastic syndrome among patients with pancytopenia. Acta Haematol 2003; 109:212-3.
77. Flores-Figueroa E, Arana-Trejo RM, Gutierrez-Espindola G, Perez-Cabrera A, Mayani H. Mesenchymal stem cells in myelodysplastic syndromes: phenotypic and cytogenetic characterization. Leuk Res 2005; 29:215-24. (Pubitemid 39647516)
78. Mayani H. Abnormal stromal cells in myelodysplastic syndromes: genomics presents further evidence. Leuk Res 2007; 31:577-8.
79. Gersuk GM, Lee JW, Beckham CA, Anderson J, Deeg HJ. Fas (CD95) receptor and Fas-ligand expression in bone marrow cells from patients with myelodysplastic syndrome. Blood 1996; 88:1122-3. (Pubitemid 26333341)
80. Gersuk GM, Beckham C, Loken MR, Kiener P, Anderson JE, Farrand A, et al. A role for tumour necrosis factor-alpha, Fas and Fas-Ligand in marrow failure associated with myelodysplastic syndrome. Br J Haematol 1998; 103:176-88.
81. Kitagawa M, Yamaguchi S, Takahashi M, Tanizawa T, Hirokawa K, Kamiyama R. Localization of Fas and Fas ligand in bone marrow cells demonstrating myelodysplasia. Leukemia 1998; 12:486-92.
82. Bouscary D, Chen YL, Guesnu M, Picard F, Viguier F, Lacombe C, et al. Activity of the caspase-3/CPP32 enzyme is increased in "early stage" myelodysplastic syndromes with excessive apoptosis, but caspase inhibition does not enhance colony formation in vitro. Exp Hematol 2000; 28:784-91.
83. Houwerzijl EJ, Blom NR, van der Want JJ, Louwes H, Esselink MT, Smit JW, et al. Increased peripheral platelet destruction and caspase-3-independent programmed cell death of bone marrow megakaryocytes in myelodysplastic patients. Blood 2005; 105:3472-9.
84. Parker JE, Mufti GJ, Rasool F, Mijovic A, Devereux S, Pagliuca A. The role of apoptosis, proliferation and the Bcl-2-related proteins in the myelodysplastic syndromes and acute myeloid leukemia secondary to MDS. Blood 2000; 96:3932-8.
85. + cells in patients with myelodysplastic syndrome: correlation with apoptosis. Leukemia 2003; 17:2460-6.
86. Kerbauy DM, Lesnikov V, Abbasi N, Seal S, Scott B, Deeg HJ. NFkappaB and FLIP in arsenic trioxide (ATO)-induced apoptosis in myelodysplastic syndromes (MDSs). Blood 2005; 106:3917-25.
87. Konen E, Ghoti H, Goitein O, Winder A, Kushnir T, Eshet Y, et al. No evidence for myocardial iron overload in multitransfused patients with myelodysplastic syndrome using cardiac magnetic resonance T2 technique. Am J Hematol 2007; 82:1013-6. (Pubitemid 350004394)
88. Yoshida S, Kuriyama K, Miyazaki Y, Taguchi J, Fukushima T, Honda M, et al. De novo acute myeloid leukemia in the elderly; a consistent fraction of long-term survivors by standard-dose chemotherapy. Leuk Res 2001; 25:33-8.
89. Novotna B, Bagryantseva Y, Siskova M, Neuwirtova R. Oxidative DNA damage in bone marrow cells of patients with low-risk myelodysplastic syndrome. Leuk Res 2009; 33:340-3.
90. Glassner BJ, Rasmussen LJ, Najarian MT, Posnick LM, Samson LD. Generation of a strong mutator phenotype in yeast by imbalanced base excision repair. Proc Natl Acad Sci U S A1998; 95:9997-10002.
91. Harada S, Komatsu H, Seto M, Ni H, Xu JH, Hayami Y, et al. Microsatellite instability is rare in the clinical course of myelodysplastic syndrome studied with DNA from fresh and paraffin-embedded tissues. J Cancer Res Clin Oncol 1998; 124:231-5.
92. + myelodysplastic syndrome marrow cells to disease subtype and progression. Blood 2009; 114:4847-58.
93. + cells in early and advanced myelodysplastic syndrome. Neoplasma 2009; 56:335-42.
94. + cells from patients with early and advanced myelodysplastic syndrome. Leuk Res 2010; [Epub ahead of print].
95. Mendiburu CF, Silva WA Jr, Ricci O Jr, Bonini-Domingos CR, Fett-Conte AC. Global gene expression profile in myelodysplastic syndromes using SAGE. Genet Mol Res 2008; 7:1245-50.
96. Qian J, Chen Z, Wang W, Cen J, Xue Y. Gene expression profiling of the bone marrow mononuclear cells from patients with myelodysplastic syndrome. Oncol Rep 2005; 14:1189-97.
97. Chen G, Zeng W, Miyazato A, Billings E, Maciejewski JP, Kajigaya S, et al. Distinctive gene expression profiles of CD34 cells from patients with myelodysplastic syndrome characterized by specific chromosomal abnormalities. Blood 2004; 104:4210-8.
98. Pellagatti A, Esoof N, Watkins F, Langford CF, Vetrie D, Campbell LJ, et al. Gene expression profiling in the myelodysplastic syndromes using cDNA microarray technology. Br J Haematol 2004; 125:576-83.
99. Ueda M, Ota J, Yamashita Y, Choi YL, Ohki R, Wada T, et al. DNA microarray analysis of stage progression mechanism in myelodysplastic syndrome. Br J Haematol 2003; 123:288-96. (Pubitemid 37305064)
100. Pellagatti A, Cazzola M, Giagounidis A, Perry J, Malcovati L, Della Porta MG, et al. Deregulated gene expression pathways in myelodysplastic syndrome hematopoietic stem cells. Leukemia 2010; 24:756-64.
101. Haase D, Germing U, Schanz J, Pfeilstocker M, Nosslinger T, Hildebrandt B, et al. New insights into the prognostic impact of the karyotype in MDS and correlation with subtypes: evidence from a core dataset of 2,124 patients. Blood 2007; 110:4385-95.
102. O'Keefe C, McDevitt MA, Maciejewski JP. Copy neutral loss of heterozygosity: a novel chromosomal lesion in myeloid malignancies. Blood 2010; 115:2731-9.